Poly(ADP-ribosylation) and neurodegenerative disorders

Mitochondrion

Volumn 24, Issue , 2015, Pages 56-63

  Basello, Davide Alessandro ^a   Scovassi, Anna Ivana ^a  

^a CNR   (Italy)

Author keywords

Apoptosis; Mitochondria; Mitophagy; Neurodegeneration; Parthanatos; Poly(ADP ribosylation)

Indexed keywords

APOPTOSIS INDUCING FACTOR; GLYCOSIDASE; MITOCHONDRIAL DNA; N METHYL DEXTRO ASPARTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); REACTIVE OXYGEN METABOLITE; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; POLY(ADP)-RIBOSYLATED PROTEINS; PROTEIN;

AGING; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; ASTROCYTE; AUTOPHAGY; BRAIN ISCHEMIA; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL SURVIVAL; DEGENERATIVE DISEASE; DNA DEGRADATION; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME SYNTHESIS; HUMAN; HUNTINGTON CHOREA; INTRACELLULAR SIGNALING; MEMBRANE PERMEABILITY; MITOCHONDRIAL GENOME; MITOCHONDRION; MITOPHAGY; MOLECULAR INTERACTION; NECROPTOSIS; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PARTHANATOS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROCESSING; REVIEW; METABOLISM; PATHOLOGY;

CELL DEATH; HUMANS; MITOCHONDRIAL PROTEINS; NEURODEGENERATIVE DISEASES; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; PROTEINS;

EID: 84937862063     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2015.07.005     Document Type: Review

References (154)

1. Abeti R., Abramov A.Y., Duchen M.R. Beta-amyloid activates PARP causing astrocytic metabolic failure and neuronal death. Brain 2011, 134:1658-1672.
2. Akbari M., Morevati M., Croteau D., Bohr V.A. The role of DNA base excision repair in brain homeostasis and disease. DNA Repair 2015, 10.1016/j.dnarep.2015.04.029.
3. Andrabi S.A., Kang H.C., Haince J.F., Lee Y.I., Zhang J., Chi Z., et al. Iduna protects the brain from glutamate excitotoxicity and stroke by interfering with poly(ADP-ribose) polymer-induced cell death. Nat. Med. 2011, 17:692-699.
4. Anilkumar U., Prehn J.H. Anti-apoptotic BCL-2 family proteins in acute neural injury. Front. Cell. Neurosci. 2014, 8:281.
5. Aredia F., Scovassi A.I. Involvement of PARPs in cell death. Front. Biosci. 2014, 6:308-317.
6. Aredia F., Scovassi A.I. Poly(ADP-ribose): a signaling molecule in different paradigms of cell death. Biochem. Pharmacol. 2014, 92:157-163.
7. Ashrafi G., Schwarz T.L. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 2013, 20:31-42.
8. Barkauskaite E., Brassington A., Tan E.S., Warwicker J., Dunstan M.S., Banos B., et al. Visualization of poly(ADP-ribose) bound to PARG reveals inherent balance between exo- and endo-glycohydrolase activities. Nat. Commun. 2013, 4:2164.
9. Beck C., Robert I., Reina-San-Martin B., Schreiber V., Dantzer F. Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp. Cell Res. 2014, 329:18-25.
10. Bianchetti E., Mladinic M., Nistri A. Mechanisms underlying cell death in ischemia-like damage to the rat spinal cord in vitro. Cell Death Dis. 2013, 4:e707.
11. Brunyanszki A., Olah G., Coletta C., Szczesny B., Szabo C. Regulation of mitochondrial poly(ADP-Ribose) polymerase activation by the β-adrenoceptor/cAMP/protein kinase A axis during oxidative stress. Mol. Pharmacol. 2014, 86:450-462.
12. +. FEBS J. 2005, 272:4576-4589.
13. Bürkle A., Virág L. Poly(ADP-ribose): PARadigms and PARadoxes. Mol. Asp. Med. 2013, 34:1046-1065.
14. Burté F., Carelli V., Chinnery P.F., Yu-Wai-Man P. Disturbed mitochondrial dynamics and neurodegenerative disorders. Nat. Rev. Neurol. 2015, 11:11-24.
15. Caiafa P., Guastafierro T., Zampieri M. Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns. FASEB J. 2009, 23:672-678.
16. Cavone L., Chiarugi A. Targeting poly(ADP-ribose) polymerase-1 as a promising approach for immunomodulation in multiple sclerosis?. Trends Mol. Med. 2012, 18:92-100.
17. Cazzalini O., Donà F., Savio M., Tillhon M., Maccario C., Perucca P., et al. p21CDKN1A participates in base excision repair by regulating the activity of poly(ADP-ribose) polymerase-1. DNA Repair 2010, 9:627-635.
18. Cha M.Y., Kim D.K., Mook-Jung I. The role of mitochondrial DNA mutation on neurodegenerative diseases. Exp. Mol. Med. 2015, 47:e150.
19. Chavez-Valdez R., Martin L.J., Flock D.L., Northington F.J. Necrostatin-1 attenuates mitochondrial dysfunction in neurons and astrocytes following neonatal hypoxia-ischemia. Neuroscience 2012, 219:192-203.
20. Chen S., Zhang X., Song L., Le W. Autophagy dysregulation in amyotrophic lateral sclerosis. Brain Pathol. 2012, 22:110-116.
21. Chen H., Ruiz P.D., Novikov L., Casill A.D., Park J.W., Gamble M.J. MacroH2A1.1 and PARP-1 cooperate to regulate transcription by promoting CBP-mediated H2B acetylation. Nat. Struct. Mol. Biol. 2014, 21:981-989.
22. Chen Z.T., Zhao W., Qu S., Li L., Lu X.D., Su F., et al. PARP-1 promotes autophagy via the AMPK/mTOR pathway in CNE-2 human nasopharyngeal carcinoma cells following ionizing radiation, while inhibition of autophagy contributes to the radiation sensitization of CNE-2 cells. Mol. Med. Rep. 2015, 10.3892/mmr.2015.3604.
23. Chiarugi A., Dölle C., Felici R., Ziegler M. The NAD metabolome - a key determinant of cancer cell biology. Nat. Rev. Cancer 2012, 12:741-752.
24. Cho-Park P.F., Steller H. Proteasome regulation by ADP-ribosylation. Cell 2013, 153:614-627.
25. Christofferson D.E., Yuan J. Necroptosis as an alternative form of programmed cell death. Curr. Opin. Cell Biol. 2010, 22:263-268.
26. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
27. Ciechanover A., Kwon Y.T. Degradation of misfolded proteins in neurodegenerative diseases: therapeutic targets and strategies. Exp. Mol. Med. 2015, 47:e147.
28. Curtin N.J., Szabo C. Therapeutic applications of PARP inhibitors: anticancer therapy and beyond. Mol. Asp. Med. 2013, 34:1217-1256.
29. Dantzer F., Santoro R. The expanding role of PARPs in the establishment and maintenance of heterochromatin. FEBS J. 2013, 280:3508-3518.
30. Daugas E., Nochy D., Ravagnan L., Loeffler M., Susin S.A., Zamzami N., et al. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 2000, 476:118-123.
31. David K.K., Andrabi S.A., Dawson T.M., Dawson V.L. Parthanatos, a messenger of death. Front. Biosci. 2009, 14:1116-1128.
32. Dawson T.M., Dawson V.L. Molecular pathways of neurodegeneration in Parkinson's disease. Science 2003, 302:819-822.
33. De Vos M., Schreiber V., Dantzer F. The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochem. Pharmacol. 2012, 84:137-146.
34. Declercq W., Vanden Berghe T., Vandenabeele P. RIP kinases at the crossroads of cell death and survival. Cell 2009, 138:229-232.
35. Deeks E.D. Olaparib: first global approval. Drugs 2015, 75:231-240.
36. Dengjel J., Abeliovich H. Musical chairs during mitophagy. Autophagy 2014, 10:706-707.
37. Di Lisa F., Ziegler M. Pathophysiological relevance of mitochondria in NAD(+) metabolism. FEBS Lett. 2001, 492:4-8.
38. Dölle C., Niere M., Lohndal E., Ziegler M. Visualization of subcellular NAD pools and intra-organellar protein localization by poly-ADP-ribose formation. Cell. Mol. Life Sci. 2010, 67:433-443.
39. Dölle C., Rack J.G., Ziegler M. NAD and ADP-ribose metabolism in mitochondria. FEBS J. 2013, 280:3530-3541.
40. Esteves A.R.F., Domingues F.A., Janua C., Swerdlow R.H., Oliveira C.R., Cardoso S.M. Mitochondrial function in Parkinson's disease cybrids containing an nt2 neuron-like nuclear background. Mitochondrion 2008, 8:219-228.
41. Esteves A.R., Gozes I., Cardoso S.M. The rescue of microtubule-dependent traffic recovers mitochondrial function in Parkinson's disease. Biochim. Biophys. Acta 2014, 1842:7-21.
42. Ethier C., Tardif M., Arul L., Poirier G.G. PARP-1 modulation of mTOR signaling in response to a DNA alkylating agent. PLoS One 2012, 7:e47978.
43. Fang E.F., Scheibye-Knudsen M., Brace L.E., Kassahun H., SenGupta T., Nilsen H., et al. Defective mitophagy in XPA via PARP-1 hyperactivation and NAD(+)/SIRT1 reduction. Cell 2014, 157:882-896.
44. Fatokun A.A., Dawson V.L., Dawson T.M. Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities. Br. J. Pharmacol. 2014, 171:2000-2016.
45. Feng X., Koh D.W. Roles of poly(ADP-ribose) glycohydrolase in DNA damage and apoptosis. Int. Rev. Cell Mol. Biol. 2013, 304:227-281.
46. Feng D., Liu L., Zhu Y., Chen Q. Molecular signaling toward mitophagy and its physiological significance. Exp. Cell Res. 2013, 319:1697-1705.
47. Fischer J.M., Popp O., Gebhard D., Veith S., Fischbach A., Beneke S., et al. Poly(ADP-ribose)-mediated interplay of XPA and PARP1 leads to reciprocal regulation of protein function. FEBS J. 2014, 281:3625-3641.
48. Frouin I., Maga G., Denegri M., Riva F., Savio M., Spadari S., et al. Human proliferating cell nuclear antigen, poly(ADP-ribose) polymerase-1, and p21waf1/cip1. A dynamic exchange of partners. J. Biol. Chem. 2003, 278:39265-39268.
49. Galluzzi L., Kroemer G. Necroptosis: a specialized pathway of programmed necrosis. Cell 2008, 135:1161-1163.
50. Gerace E., Landucci E., Scartabelli T., Moroni F., Chiarugi A., Pellegrini-Giampietro D.E. Interplay between histone acetylation/deacetylation and poly(ADP-ribosyl)ation in the development of ischemic tolerance in vitro. Neuropharmacology 2015, 92:125-134.
51. Ghavami S., Shojaei S., Yeganeh B., Ande S.R., Jangamreddy J.R., Mehrpour M., et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog. Neurobiol. 2014, 112:24-49.
52. Giansanti V., Donà F., Tillhon M., Scovassi A.I. PARP inhibitors: new tools to protect from inflammation. Biochem. Pharmacol. 2010, 80:1869-1877.
53. Gibson B.A., Kraus W.L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 2012, 13:411-424.
54. Giménez-Cassina A., Danial N.N. Regulation of mitochondrial nutrient and energy metabolism by BCL-2 family proteins. Trends Endocrinol. Metab. 2015, 26:165-175.
55. Goldman S.J., Taylor R., Zhang Y., Jin S. Autophagy and the degradation of mitochondria. Mitochondrion 2010, 10:309-315.
56. Gomes L.C., Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys. Acta 2013, 1833:205-212.
57. Green D.R., Galluzzi L., Kroemer G. Cell biology. Metabolic control of cell death. Science 2014, 345:1250256.
58. Guamán Ortiz L.M., Giansanti V., Donà F., Scovassi A.I. Pharmacological effects of PARP inhibitors on cancer and other diseases. Curr. Enzym. Inhib. 2011, 7:244-258.
59. Hassa P.O., Hottiger M.O. The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci. 2008, 13:3046-3082.
60. He S., Wang L., Miao L., Wang T., Du F., Zhao L., et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 2009, 137:1100-1111.
61. Heeres J.T., Hergenrother P.J. Poly(ADP-ribose) makes a date with death. Curr. Opin. Chem. Biol. 2007, 11:644-653.
62. Hegedus C., Virág L. Inputs and outputs of poly(ADP-ribosyl)ation: relevance to oxidative stress. Redox Biol. 2014, 2:978-982.
63. Hitomi J., Christofferson D.E., Ng A., Yao J., Degterev A., Xavier R.J., et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 2008, 135:1311-1323.
64. Humphries F., Yang S., Wang B., Moynagh P.N. RIP kinases: key decision makers in cell death and innate immunity. Cell Death Differ. 2015, 22:225-236.
65. Izhar L., Adamson B., Ciccia A., Lewis J., Pontano-Vaites L., Leng Y., et al. A systematic analysis of factors localized to damaged chromatin reveals PARP-dependent recruitment of transcription factors. Cell Rep. 2015, 10.1016/j.celrep.2015.04.053.
66. Ji Y., Tulin A.V. Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins. Int. J. Mol. Sci. 2013, 14:16168-16183.
67. Johri A., Chandra A., Beal M.F. PGC-1α, mitochondrial dysfunction, and Huntington's disease. Free Radic. Biol. Med. 2013, 62:37-46.
68. Jouan-Lanhouet S., Arshad M.I., Piquet-Pellorce C., Martin-Chouly C., Le Moigne-Muller G., Van Herreweghe F., et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ. 2012, 19:2003-2014.
69. Kauppinen T.M., Swanson R.A. The role of poly(ADP-ribose) polymerase-1 in CNS disease. Neuroscience 2007, 145:1267-1272.
70. Khalil B., El Fissi N., Aouane A., Cabirol-Pol M.J., Rival T., Liévens J.C. PINK1-induced mitophagy promotes neuroprotection in Huntington's disease. Cell Death Dis. 2015, 6:e1617.
71. Kim T.W., Cho H.M., Choi S.Y., Suguira Y., Hayasaka T., Setou M., et al. (ADP-ribose) polymerase 1 and AMP-activated protein kinase mediate progressive dopaminergic neuronal degeneration in a mouse model of Parkinson's disease. Cell Death Dis. 2013, 4:e919.
72. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
73. +-dependent signalling. FEBS Lett. 2011, 585:1651-1656.
74. Koh D.W., Dawson T.M., Dawson V.L. Poly(ADP-ribosyl)ation regulation of life and death in the nervous system. Cell. Mol. Life Sci. 2005, 62:760-768.
75. Krantic S., Mechawar N., Reix S., Quirion R. Molecular basis of programmed cell death involved in neurodegeneration. Trends Neurosci. 2005, 28:670-676.
76. Kraus W.L., Hottiger M.O. PARP-1 and gene regulation: progress and puzzles. Mol. Asp. Med. 2013, 34:1109-1123.
77. Kraus W.L., Lis J.T. PARP goes transcription. Cell 2003, 113:677-683.
78. Krietsch J., Rouleau M., Pic E., Ethier C., Dawson T.M., Dawson V.L., et al. Reprogramming cellular events by poly(ADP-ribose)-binding proteins. Mol. Asp. Med. 2013, 34:1066-1087.
79. Krukenberg K.A., Kim S., Tan E.S., Maliga Z., Mitchison T.J. Extracellular poly(ADP-ribose) is a pro-inflammatory signal for macrophages. Chem. Biol. 2015, 22:446-452.
80. Kubli D.A., Gustafsson Å.B. Mitochondria and mitophagy: the yin and yang of cell death control. Circ. Res. 2012, 111:1208-1221.
81. Lapucci A., Pittelli M., Rapizzi E., Felici R., Moroni F., Chiarugi A. Poly(ADP-ribose) polymerase-1 is a nuclear epigenetic regulator of mitochondrial DNA repair and transcription. Mol. Pharmacol. 2011, 79:932-940.
82. Lee Y., Kang H.C., Lee B.D., Lee Y.I., Kim Y.P., Shin J.H. Poly (ADP-ribose) in the pathogenesis of Parkinson's disease. BMB Rep. 2014, 47:424-432.
83. Li N., Chen J. ADP-ribosylation: activation, recognition, and removal. Mol. Cells 2014, 37:9-16.
84. Li X., Klaus J.A., Zhang J., Xu Z., Kibler K.K., Andrabi S.A., et al. Contributions of poly(ADP-ribose) polymerase-1 and -2 to nuclear translocation of apoptosis-inducing factor and injury from focal cerebral ischemia. J. Neurochem. 2010, 113:1012-1022.
85. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
86. Linkermann A., Green D.R. Necroptosis. N. Engl. J. Med. 2014, 370:455-465.
87. Liu Q., Qiu J., Liang M., Golinski J., van Leyen K., Jung J.E., et al. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis. 2014, 5:e1084.
88. Lopez J., Tait S.W. Mitochondrial apoptosis: killing cancer using the enemy within. Br. J. Cancer 2015, 112:957-962.
89. + metabolism and NAD(+)-dependent enzymes: promising therapeutic targets for neurological diseases. Curr. Drug Targets 2012, 13:222-229.
90. Mansoorabadi S.O., Wu M., Tao Z., Gao P., Pingali S.V., Guo L., et al. Conformational activation of poly(ADP-ribose) polymerase-1 upon DNA binding revealed by small-angle X-ray scattering. Biochemistry 2014, 53:1779-1788.
91. Marshall K.D., Baines C.P. Necroptosis: is there a role for mitochondria?. Front. Physiol. 2014, 5:323.
92. Martire S., Mosca L., d'Erme M. PARP-1 involvement in neurodegeneration: a focus on Alzheimer's and Parkinson's diseases. Mech. Ageing Dev. 2015, 146-148C:53-64.
93. Mazzone G.L., Nistri A. Effect of the PARP-1 inhibitor PJ 34 on excitotoxic damage evoked by kainate on rat spinal cord organotypic slices. Cell. Mol. Neurobiol. 2011, 31:469-478.
94. McLelland G.L., Soubannier V., Chen C.X., McBride H.M., Fon E.A. Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J. 2014, 33:282-295.
95. Meyer R.G., Meyer-Ficca M.L., Whatcott C.J., Jacobson E.L., Jacobson M.K. Two small enzyme isoforms mediate mammalian mitochondrial poly(ADP-ribose) glycohydrolase (PARG) activity. Exp. Cell Res. 2007, 313:2920-2936.
96. Muñoz-Gámez J.A., Rodríguez-Vargas J.M., Quiles-Pérez R., Aguilar-Quesada R., Martín-Oliva D., de Murcia G., et al. PARP-1 is involved in autophagy induced by DNA damage. Autophagy 2009, 5:61-74.
97. Murphy J.M., Silke J. Ars Moriendi; the art of dying well - new insights into the molecular pathways of necroptotic cell death. EMBO Rep. 2014, 15:155-164.
98. Nasrabady S.E., Kuzhandaivel A., Mladinic M., Nistri A. Effects of 6(5H)-phenanthridinone, an inhibitor of poly(ADP-ribose)polymerase-1 activity (PARP-1), on locomotor networks of the rat isolated spinal cord. Cell. Mol. Neurobiol. 2011, 31:503-508.
99. Nassif M., Valenzuela V., Rojas-Rivera D., Vidal R., Matus S., Castillo K., et al. Pathogenic role of BECN1/Beclin 1 in the development of amyotrophic lateral sclerosis. Autophagy 2014, 10:1256-1271.
100. Niere M., Kernstock S., Koch-Nolte F., Ziegler M. Functional localization of two poly(ADP-ribose)-degrading enzymes to the mitochondrial matrix. Mol. Cell. Biol. 2008, 28:814-824.
101. Niere M., Mashimo M., Agledal L., Dölle C., Kasamatsu A., Kato J., et al. ADP-ribosylhydrolase 3 (ARH3), not poly(ADP-ribose) glycohydrolase (PARG) isoforms, is responsible for degradation of mitochondrial matrix-associated poly(ADP-ribose). J. Biol. Chem. 2012, 287:16088-16102.
102. Nikoletopoulou V., Papandreou M.E., Tavernarakis N. Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ. 2015, 22:398-407.
103. Ofengeim D., Yuan J. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 2013, 14:727-736.
104. +-induced cytotoxicity in Parkinson's disease in vitro models. Biochem. Biophys. Res. Commun. 2007, 357:596-602.
105. Park E.J., Min K.J., Lee T.J., Yoo Y.H., Kim Y.S., Kwon T.K. β-Lapachone induces programmed necrosis through the RIP1-PARP-AIF-dependent pathway in human hepatocellular carcinoma SK-Hep1 cells. Cell Death Dis. 2014, 5:e1230.
106. Pines A., Mullenders L.H., van Attikum H., Luijsterburg M.S. Touching base with PARPs: moonlighting in the repair of UV lesions and double-strand breaks. Trends Biochem. Sci. 2013, 38:321-330.
107. Pinho C.M., Teixeira P.F., Glaser E. Mitochondrial import and degradation of amyloid-β peptide. Biochim. Biophys. Acta 2014, 1837:1069-1074.
108. Re D.B., Le Verche V., Yu C., Amoroso M.W., Politi K.A., Phani S., et al. Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 2014, 81:1001-1008.
109. Realini C.A., Althaus F.R. Histone shuttling by poly(ADP-ribosylation). J. Biol. Chem. 1992, 267:18858-18865.
110. Rodriguez-Vargas J.M., Ruiz-Magana M.J., Ruiz-Ruiz C., Majuelos-Melguizo J., Peralta-Leal A., Rodriguez M.I., et al. ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell Res. 2012, 22:1181-1198.
111. Rolland S.G., Conradt B. New role of the BCL2 family of proteins in the regulation of mitochondrial dynamics. Curr. Opin. Cell Biol. 2010, 22:852-858.
112. Rosenbaum D.M., Degterev A., David J., Rosenbaum P.S., Roth S., Grotta J.C., et al. Necroptosis, a novel form of caspase-independent cell death, contributes to neuronal damage in a retinal ischemia-reperfusion injury model. J. Neurosci. Res. 2010, 88:1569-1576.
113. Rossi M.N., Carbone M., Mostocotto C., Mancone C., Tripodi M., Maione R., et al. Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J. Biol. Chem. 2009, 284:31616-31624.
114. Ryu K.W., Kim D.S., Kraus W.L. New facets in the regulation of gene expression by ADP-ribosylation and poly(ADP-ribose) polymerases. Chem. Rev. 2015, 115:2453-2481.
115. Salminen A., Kaarniranta K., Kauppinen A., Ojala J., Haapasalo A., Soininen H., et al. Impaired autophagy and APP processing in Alzheimer's disease: the potential role of Beclin 1 interactome. Prog. Neurobiol. 2013, 106-107:33-54.
116. Sarkar S., Ravikumar B., Rubinsztein D.C. Autophagic clearance of aggregate-prone proteins associated with neurodegeneration. Methods Enzymol. 2009, 453:83-110.
117. Scarffe L.A., Stevens D.A., Dawson V.L., Dawson T.M. Parkin and PINK1: much more than mitophagy. Trends Neurosci. 2014, 37:315-324.
118. Schapira A.H., Olanow C.W., Greenamyre J.T., Bezard E. Slowing of neurodegeneration in Parkinson's disease and Huntington's disease: future therapeutic perspectives. Lancet 2014, 384:545-555.
119. Scheibye-Knudsen M., Fang E.F., Croteau D.L., Bohr V.A. Contribution of defective mitophagy to the neurodegeneration in DNA repair-deficient disorders. Autophagy 2014, 10:1468-1469.
120. Scovassi A.I. Mitochondrial poly(ADP-ribosylation): from old data to new perspectives. FASEB J. 2004, 18:1487-1488.
121. Sharifi R., Morra R., Appel C.D., Tallis M., Chioza B., Jankevicius G., et al. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenerative disease. EMBO J. 2013, 32:1225-1237.
122. Shen H.M., Codogno P. Autophagic cell death: Loch Ness monster or endangered species?. Autophagy 2011, 7:457-465.
123. Smigrodzki R.M., Khan S.M. Mitochondrial microheteroplasmy and a theory of aging and age-related disease. Rejuvenation Res. 2005, 8:172-198.
124. Sosna J., Voigt S., Mathieu S., Lange A., Thon L., Davarnia P., et al. TNF-induced necroptosis and PARP-1-mediated necrosis represent distinct routes to programmed necrotic cell death. Cell. Mol. Life Sci. 2014, 71:331-348.
125. Sun L., Wang X. A new kind of cell suicide: mechanisms and functions of programmed necrosis. Trends Biochem. Sci. 2014, 39:587-593.
126. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
127. Swerdlow R.H. Does mitochondrial DNA play a role in Parkinson's disease? A review of cybrid and other supportive evidence. Antioxid. Redox Signal. 2012, 16:950-964.
128. Swerdlow R.H., Khan S.M. A "mitochondrial cascade hypothesis" for sporadic Alzheimer's disease. Med. Hypotheses 2004, 63:8-20.
129. Swerdlow R.H., Parks J.K., Miller S.W., Tuttle J.B., Trimmer P.A., Sheehan J.P., et al. Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 1996, 40:663-671.
130. Swerdlow R.H., Parks J.K., Cassarino D.S., Maguire D.J., Maguire R.S., Bennett J.P., et al. Cybrids in Alzheimer's disease: a cellular model of the disease?. Neurology 1997, 49:918-925.
131. Swerdlow R.H., Burns J.M., Khan S.M. The Alzheimer's disease mitochondrial cascade hypothesis: progress and perspectives. Biochim. Biophys. Acta 2014, 1842:1219-1231.
132. Szczesny B., Brunyanszki A., Olah G., Mitra S., Szabo C. Opposing roles of mitochondrial and nuclear PARP1 in the regulation of mitochondrial and nuclear DNA integrity: implications for the regulation of mitochondrial function. Nucleic Acids Res. 2014, 42:13161-13173.
133. Tallis M., Morra R., Barkauskaite E., Ahel I. Poly(ADP-ribosyl)ation in regulation of chromatin structure and the DNA damage response. Chromosoma 2014, 123:79-90.
134. Tatsuta T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 2008, 27:306-314.
135. Turunc Bayrakdar E., Uyanikgil Y., Kanit L., Koylu E., Yalcin A. Nicotinamide treatment reduces the levels of oxidative stress, apoptosis, and PARP-1 activity in Aβ(1-42)-induced rat model of Alzheimer's disease. Free Radic. Res. 2014, 48:146-158.
136. Vanden Berghe T., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 2014, 15:135-147.
137. Vandenabeele P., Galluzzi L., Vanden Berghe T., Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11:700-714.
138. Venderova K., Park D.S. Programmed cell death in Parkinson's disease. Cold Spring Harb. Perspect. Med. 2012, 2:a009365.
139. Virág L., Robaszkiewicz A., Vargas J.M., Oliver J.F. Poly(ADP-ribose) signaling in cell death. Mol. Asp. Med. 2013, 34:1153-1167.
140. Vives-Bauza C., Przedborski S. Mitophagy: the latest problem for Parkinson's disease. Trends Mol. Med. 2011, 17:158-165.
141. Wang K., Klionsky D.J. Mitochondria removal by autophagy. Autophagy 2011, 7:297-300.
142. Wu X.L., Wang P., Liu Y.H., Xue Y.X. Effects of poly (ADP-ribose) polymerase inhibitor 3-aminobenzamide on blood-brain barrier and dopaminergic neurons of rats with lipopolysaccharide-induced Parkinson's disease. J. Mol. Neurosci. 2014, 53:1-9.
143. Xu Y., Huang S., Liu Z.G., Han J. Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J. Biol. Chem. 2006, 281:8788-8795.
144. Xu X., Chua C.C., Zhang M., Geng D., Liu C.F., Hamdy R.C., et al. The role of PARP activation in glutamate-induced necroptosis in HT-22 cells. Brain Res. 2010, 1343:206-212.
145. Xu H., Luo P., Zhao Y., Zhao M., Yang Y., Chen T., et al. Iduna protects HT22 cells from hydrogen peroxide-induced oxidative stress through interfering poly(ADP-ribose) polymerase-1-induced cell death (parthanatos). Cell. Signal. 2013, 25:1018-1026.
146. Yokoyama H., Kuroiwa H., Tsukada T., Uchida H., Kato H., Araki T. Poly(ADP-ribose)polymerase inhibitor can attenuate the neuronal death after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity in mice. J. Neurosci. Res. 2010, 88:1522-1536.
147. Youle R.J., Narendra D.P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 2011, 12:9-14.
148. Yu S.W., Andrabi S.A., Wang H., Kim N.S., Poirier G.G., Dawson T.M., et al. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18314-18319.
149. Zhang L., Jiang F., Chen Y., Luo J., Liu S., Zhang B., et al. Necrostatin-1 attenuates ischemia injury induced cell death in rat tubular cell line NRK-52E through decreased Drp1 expression. Int. J. Mol. Sci. 2013, 14:24742-24754.
150. Zhou W., Yuan J. Necroptosis in health and diseases. Semin. Cell Dev. Biol. 2014, 35:14-23.
151. Zhou Z.R., Zhu X.D., Zhao W., Qu S., Su F., Huang S.T., et al. Poly(ADP-ribose) polymerase-1 regulates the mechanism of irradiation-induced CNE-2 human nasopharyngeal carcinoma cell autophagy and inhibition of autophagy contributes to the radiation sensitization of CNE-2 cells. Oncol. Rep. 2013, 29:2498-2506.
152. Zhu J., Wang K.Z., Chu C.T. After the banquet: mitochondrial biogenesis, mitophagy, and cell survival. Autophagy 2013, 9:1663-1676.
153. http://ghr.nlm.nih.gov/glossary=heteroplasmy.
154. http://www.neurodegenerationresearch.eu/about/what.